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The Application of Ozonated Water Rearranges the Vitis Vinifera L. Leaf and Berry Transcriptomes Eliciting Defence and Antioxida

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The Application of Ozonated Water Rearranges the Vitis Vinifera L. Leaf and Berry Transcriptomes Eliciting Defence and Antioxida www.nature.com/scientificreports OPEN The application of ozonated water rearranges the Vitis vinifera L. leaf and berry transcriptomes eliciting defence and antioxidant responses Ana Campayo1,2,5, Stefania Savoi3,5, Charles Romieu3, Alberto José López‑Jiménez4, Kortes Serrano de la Hoz2, M. Rosario Salinas1, Laurent Torregrosa3* & Gonzalo L. Alonso1 Ozonated water has become an innovative, environmentally friendly tool for controlling the development of fungal diseases in the vineyard or during grape postharvest conservation. However, little information is currently available on the efects of ozonated water sprayings on the grapevine physiology and metabolism. Using the microvine model, we studied the transcriptomic response of leaf and fruit organs to this treatment. The response to ozone was observed to be organ and developmental stage‑dependent, with a decrease of the number of DEGs (diferentially expressed genes) in the fruit from the onset of ripening to later stages. The most highly up‑regulated gene families were heat‑shock proteins and chaperones. Other up‑regulated genes were involved in oxidative stress homeostasis such as those of the ascorbate–glutathione cycle and glutathione S‑transferases. In contrast, genes related to cell wall development and secondary metabolites (carotenoids, terpenoids, phenylpropanoids / favonoids) were generally down‑regulated after ozone treatment, mainly in the early stage of fruit ripening. This down‑regulation may indicate a possible carbon competition favouring the re‑establishment and maintenance of the redox homeostasis rather than the synthesis of secondary metabolites at the beginning of ripening, the most ozone responsive developmental stage. Vitis vinifera encompasses most grapevine cultivars used for table grape and wine production. Unfortunately, this species is highly susceptible to a range of fungal diseases such as downy and powdery mildews and the grey mould, respectively caused by Plasmopara viticola, Erysiphe necator and Botrytis cinerea. Moreover, a complex group of pathogenic fungi that attacks perennial organs is responsible for the so-called grapevine trunk diseases. To overcome the negative impacts of these pathogens on plant development and fruit quality, and avoid excessive crop losses, viticulture needs to perform intense fungicide spraying programs, especially in hot and wet weather conditions. Even organic and biodynamic approaches largely require sulfur- and copper-based formulations that may be detrimental to the soil ecosystem in the long term. Te ecological and environmental sustainability is an increasing concern for consumers and more generally for society. One way to reduce the susceptibility of V. vinifera to pathogens is to breed new cultivars introgressing genetic traits of resistance from American and Asian Vitis spp. Several breeding programs are ongoing in Europe and abroad with an increment of new resistant genotypes available. In parallel to introducing new varieties, which is a long process and ofen not entirely accepted by the market, other strategies like the application of bioactive natural-derived products (silicons, laminarin, potassium phosphonates, analog of salicylic acid, phytomela- 1,2 tonin, etc.) that act as elicitors of plant biotic stress resistance , or the use of ozone (O3) have been proposed as smart approaches to control fungal diseases. Indeed, when applied in aqueous solution, ozone has been shown to suppress spore germination of the esca-associated fungus Phaeoacremonium aleophilum and reduce fungal development by 50% on Cabernet Sauvignon cuttings3. Te use of ozonated water in integrated vineyard pest 1Cátedra de Química Agrícola, E.T.S.I. Agrónomos y de Montes, Universidad de Castilla-La Mancha, Avda. de España s/n, 02071 Albacete, Spain. 2BetterRID (Better Research, Innovation and Development, S.L.), Carretera de Las Peñas (CM-3203), Km 3.2, Campo de Prácticas-UCLM, 02071 Albacete, Spain. 3AGAP, CIRAD, INRAe, Institut Agro-Montpellier SupAgro, Montpellier University, 34060 Montpellier, France. 4Departamento de Ciencia y Tecnología Agroforestal y Genética, Universidad de Castilla-La Mancha, Campus Universitario s/n, 02071 Albacete, Spain. 5These authors contributed equally: Ana Campayo and Stefania Savoi. *email: laurent.torregrosa@ supagro.fr Scientifc Reports | (2021) 11:8114 | https://doi.org/10.1038/s41598-021-87542-y 1 Vol.:(0123456789) www.nature.com/scientificreports/ Figure 1. Sugar and acid content and organ fresh weight. (a) Malic acid (mEq) as a function of sugar (glucose + fructose, mM). Full coloured circles represent the individual berry or pairs of leaves selected for RNA-Seq; (b) Average concentrations in glucose + fructose (mM), malic acid (mEq), tartaric acid (mEq), and organ fresh weight (g) of the selected triplicates. Error bars represent the SD (n = 3). Selected samples showed no signifcant diferences between conditions (C and OW) according to the independent samples t-test (p < 0.05). Figure was obtained with IBM SPSS Statistics 24 (https:// www. ibm. com/ produ cts/ spss- stati stics). management appears to be as efective as traditional chemical treatments in reducing fungal populations on leaves and grape bunches4. Te efciency of ozone is thought to lie in its oxidising potential, which translates into the ability to react with numerous cellular constituents hence a broad-spectrum antimicrobial action5. Its low persistence afer application makes ozone particularly attractive from an environmental point of view. Tis triatomic molecule is highly unstable and spontaneously decomposes into oxygen without leaving hazardous residues, with a shorter half-life in water than in the gaseous state 5. In aqueous solution, ozone can be broken down via a chain reaction mechanism resulting in the production of reactive oxygen species (ROS), · · − · i.e. the hydroperoxide (HO2 ), superoxide ( O2 ) and hydroxyl ( OH) radicals and hydrogen peroxide (H2O2), all contributing to the high oxidising power of ozone6. Ozone enters plant tissues through the stomata, lenticels or physical breaks in the cuticle. Ten it reacts with molecules present in the apoplastic fuid, cell wall and plasma membranes, where it decomposes to produce the ROS mentioned above 7. Under the oxidative stress induced by ozone and derived products, plants develop defence mechanisms at the genetic, transcriptional and biochemical level, which includes the synthesis of anti- oxidants such as ascorbate, glutathione, enzymes like superoxide dismutases, catalases and peroxidases, and secondary metabolites like carotenoids, terpenoids and phenolics 8–10. When the detoxifcation capacity of plant cells is overwhelmed, cellular damage can occur. Most research about the efects of ozone on plants has focused on the physiological changes triggered by ozone as a pollutant. However, ozone applied in aqueous solution and in a timely manner is expected to interact with plants diferently than in the gaseous state, with a sufciently high phytotoxic threshold that allows its incorpo- ration in irrigation and spraying treatments in diferent crop species11. Unfortunately, literature concerning the efects of ozonated water on grapevine plants is scarce and almost exclusively dedicated to analysing its efect on microbial populations3,4,12, except a few recent studies describing its impact on grape and wine composition12–16. Te microvine is a convenient model plant for performing physiological studies in a semi-controlled environ- ment. Carrying the Vvigai1 mutation, microvines exhibit a continuous fowering, simultaneously displaying all the successive stages of fruit development on a single shoot17. Tis model has already facilitated transcriptomics approaches of the circadian cycle 18, high-temperature stresses 19,20, metabolomics works surveying glycosylated aroma precursors21,22, and several berry developmental studies23–25. In this study, this model allowed us to characterise the early transcriptome changes triggered in grapevine leaves and berries at diferent ripening stages afer in planta sprayings of ozonated water solutions. Results The balance in primary metabolites: an analytical tool to select RNA‑Seq samples. At the beginning of ripening (BR), sof green berries were sampled while still in the lag phase with no visible anthocya- nin accumulation in their skin. Tese berries just started to accumulate sugar while consuming malate (Fig. 1a). As expected, berries in the mid-ripening stage (MR) showed higher sugar concentrations (close to 1 M) and a lower amount of malic acid (Fig. 1a). Mature leaf samples (L) displayed a comparable amount of soluble sugars Scientifc Reports | (2021) 11:8114 | https://doi.org/10.1038/s41598-021-87542-y 2 Vol:.(1234567890) www.nature.com/scientificreports/ Figure 2. Transcriptomics overview. Principal component analysis of the transcriptomic samples in (a) leaves (L, green), (b) berries at the beginning of ripening (BR, orange), and (c) berries in mid-ripening (MR, purple); (d) sample dendrogram, with C and OW samples represented with a square and a triangle, respectively; (e) number of DEGs in L, BR and MR, and (f) commonly and uniquely modulated genes. to BR, with a two-fold lower malate concentration, indicating strong diferentiation between the source (leaves) and sink (berries) organs. Tanks to the measurements of sugars and acids, it was possible to gather synchronised samples26 for further RNA-Seq analysis with the aim to reduce biases in gene expression caused by the natural developmental asynchrony of grapevine berries
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